Developmental and aging changes in brain network switching dynamics revealed by EEG phase synchronization

脑电图相位同步揭示大脑网络转换动力学的发育和衰老变化

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Abstract

Adaptive behavior depends on the brain's capacity to vary its activity across multiple spatial and temporal scales. Yet, how distinct facets of this variability evolve from childhood to older adulthood remains poorly understood, limiting mechanistic models of neurocognitive aging. Here, we characterize lifespan neural variability using an integrated empirical-computational approach. We analyzed high-density EEG cohort data spanning 111 healthy individuals aged 9-75 years, recorded at rest and during a passive and an attended auditory oddball stimulation task. We extracted scale-dependent measures of EEG fluctuation amplitude and entropy, together with millisecond-resolved phase-synchrony networks in the 2-20 Hz range. Multi-condition partial least squares decomposition analysis revealed two independent lifespan trajectories. First, slow-frequency power, variance, and complexity at longer timescales declined monotonically with age, indicating a progressive dampening of low-frequency fluctuations and large-scale coherence. Second, the temporal organization of phase-synchrony reconfigurations followed an inverted U-shaped trend: young adults exhibited the slowest yet most diverse switching-characterized by low mean but high variance and low kurtosis of jump lengths at 2-6 Hz, and the opposite pattern at 8-20 Hz-whereas children and older adults showed faster, more stereotyped dynamics. To mechanistically account for these patterns, we fitted a ten-node phase-oscillator model constrained by the human structural connectome. Only an intermediate, metastable coupling regime qualitatively reproduced the empirical finding of maximally heterogeneous synchrony dynamics observed in young adults, whereas deviations toward weaker or stronger coupling mimicked the children's and older adults' profiles. Our results demonstrate that development and aging entail changes in the switching dynamics of EEG phase synchronization by differentially sculpting stationary and transient aspects of neural variability. This establishes time-resolved phase-synchrony metrics as sensitive, mechanistically grounded markers of neurocognitive status across the lifespan.

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